Hybridization plays a central role in plant evolution, but its overall importance in fungi is unknown. It has been suggested that new plant pathogens could arise by hybridization between formerly separated fungal species. Evolution of hybrid plant pathogens from non-pathogenic ancestors in the fungal-like protist <i>Phytophthora</i> has been demonstrated, but in fungi, the most important group of plant pathogens, there are few well-characterized examples of hybrids. We focused our attention on the diploid hybrid and plant pathogen <i>Verticillium longisporum</i>, the causal agent of the Verticillium wilt disease in crucifer crops. To address questions related to the evolutionary origin of <i>V. longisporum</i>, we used phylogenetic analyses of seven nuclear loci and a dataset of 203 isolates of <i>V. longisporum</i>, <i>V. dahliae</i> and related species. We confirmed that <i>V. longisporum</i> was diploid, and originated three different times, involving four different lineages and three different parental species. All hybrids shared a common parent, Species A1 that hybridized respectively with Species D1, <i>V. dahliae</i> lineage D2 and <i>V. dahliae</i> lineage D3, to give rise to three different lineages of <i>V. longisporum</i>. Species A1 and Species D1 are as yet unknown taxa. <i>Verticillium longisporum</i> likely originated recently, as each <i>V. longisporum</i> lineage was genetically homogenous, and comprised Species A1 alleles that were identical across lineages. The three different hybrid lineages may differ in virulence.<p><p>Keywords: